Population genomics reveals that an anthropophilic population of Aedes aegypti mosquitoes in West Africa recently gave rise to American and Asian populations of this major disease vector

Jacob E Crawford,William J Palmer,Jonathan P Day,Ranjan Ramasamy,Joel M Alves,Francis M Jiggins,William C Black,Massamba Sylla,Sinnathamby N Surendran,Arnab Pain

doi:10.1186/s12915-017-0351-0

Abstract

BackgroundThe mosquito Aedes aegypti is the main vector of dengue, Zika, chikungunya and yellow fever viruses. This major disease vector is thought to have arisen when the African subspecies Ae. aegypti formosus evolved from being zoophilic and living in forest habitats into a form that specialises on humans and resides near human population centres. The resulting domestic subspecies, Ae. aegypti aegypti, is found throughout the tropics and largely blood-feeds on humans.ResultsTo understand this transition, we have sequenced the exomes of mosquitoes collected from five populations from around the world. We found that Ae. aegypti specimens from an urban population in Senegal in West Africa were more closely related to populations in Mexico and Sri Lanka than they were to a nearby forest population. We estimate that the populations in Senegal and Mexico split just a few hundred years ago, and we found no evidence of Ae. aegypti aegypti mosquitoes migrating back to Africa from elsewhere in the tropics. The out-of-Africa migration was accompanied by a dramatic reduction in effective population size, resulting in a loss of genetic diversity and rare genetic variants.ConclusionsWe conclude that a domestic population of Ae. aegypti in Senegal and domestic populations on other continents are more closely related to each other than to other African populations. This suggests that an ancestral population of Ae. aegypti evolved to become a human specialist in Africa, giving rise to the subspecies Ae. aegypti aegypti. The descendants of this population are still found in West Africa today, and the rest of the world was colonised when mosquitoes from this population migrated out of Africa. This is the first report of an African population of Ae. aegypti aegypti mosquitoes that is closely related to Asian and American populations. As the two subspecies differ in their ability to vector disease, their existence side by side in West Africa may have important implications for disease transmission.

Highlights

The mosquito Aedes aegypti is the main vector of dengue, Zika, chikungunya and yellow fever viruses
Anthropophilic Ae. aegypti from Senegal are genetically distinct from other African populations and populations outside of Africa There is clear genetic structure among the five populations we studied, with principal component analysis (PCA) clustering samples from the same location together
The urban population in Senegal has the typical characteristics of the subspecies Ae. aegypti aegypti that is found throughout the tropics outside Africa: it lives alongside humans and has the characteristic pale scales on the first abdominal tergite [10, 14, 15]

Summary

Introduction

The mosquito Aedes aegypti is the main vector of dengue, Zika, chikungunya and yellow fever viruses. This major disease vector is thought to have arisen when the African subspecies Ae. aegypti formosus evolved from being zoophilic and living in forest habitats into a form that specialises on humans and resides near human population centres. Aside from a few locations on the coast of Kenya that appear to have been colonised by non-African populations, African populations tend to cluster together genetically regardless of whether they are forest or domestic forms [12] This was interpreted as suggesting that these human-associated populations in Africa have arisen independently from the domestic populations found elsewhere in the tropics [12]. As we discuss later, such interpretations of genetic data can be misleading

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